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Marine Ecology Progress Series 397:103 Vol. 397: 103–112, 2009 MARINE ECOLOGY PROGRESS SERIES Published December 17 doi: 10.3354/meps08322 Mar Ecol Prog Ser Contribution to the Theme Section ‘Conservation and management of deep-sea corals and coral reefs’ OPENPEN ACCESSCCESS Reproductive biology of the deep-sea pennatulacean Anthoptilum murrayi (Cnidaria, Octocorallia) D. O. Pires*, C. B. Castro, J. C. Silva Museu Nacional/Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, s/n, São Cristóvão, Rio de Janeiro 20940-040, Brazil ABSTRACT: Anthoptilum murrayi has been reported from the North Atlantic, northern Mid-Atlantic Ridge, Indian Ocean and in waters around New Zealand and Australia. Recently, this species was also recorded in deep waters off Brazil, southwestern Atlantic. It was from this region (13° to 22° S) that specimens were collected, in 1300 to 1799 m, to determine the reproductive biology of A. mur- rayi using histological methods. The colony polyparium was divided into 3 zones (distal, medial and basal) to evaluate differences in gamete development between zones; dissected polyps were exam- ined from the 3 zones to estimate fecundity. The species appears to display a continuous and long breeding activity rather than any seasonal reproductive pattern. Most oocytes were in the earliest stages of development and basal polyps presented the highest frequency of small eggs. The large mature oocytes (up to 1200 µm) indicate that A. murrayi produces lecithotrophic larvae. Females had 0 to 90 oocytes per polyp and 25 713 to 35 918 oocytes per colony. Male colonies of similar size to the female samples were shown to have 6 to 76 cysts per polyp and 14 014 to 27 019 cysts per colony. A. murrayi is a sessile gonochoric species with a 1:1 sex ratio and is most likely a broadcast spawner. The species has high fecundity, large eggs that could represent larger targets for sperm, primitive sper- matophores, as well as a large number of polyps per colony. These factors, along with a patchy distri- bution, would enhance the chance of fertilization for A. murrayi and may guarantee a successful reproductive strategy for this species. KEY WORDS: Pennatulacea · Gametogenesis · Fecundity · Deep-sea Resale or republication not permitted without written consent of the publisher INTRODUCTION ever, data from a larger number of octocoral species is required for any robust analysis of reproductive Knowledge of the reproductive biology of organisms biology for this group. is essential to understanding how populations can be Information on reproductive traits of deep-sea corals maintained and renewed. Data comprising, for exam- is more recent and limited. Some deep-sea studies ple, the sexuality, reproductive mode, sex ratio and impose serious restrictions on specimen data acquisi- seasonality of reproduction of species of concern are tion and many studies use material already available in crucial to the establishment of better policies for the collections and are thus not ideally preserved. As such, management, conservation and recovery strategies of there are often few temporal series making it difficult degraded areas. to present conclusive investigations on timing of the Reproduction and propagation of shallow-water gametogenic cycle, duration of gametogenesis, sea- tropical corals have been extensively studied, particu- sonality and specific dates for gamete release or plan- larly for the scleractinians (Harrison & Wallace 1990). ulation. In spite of these logistical restraints, partially The reproductive biology of octocorals has also fo- accumulated data can show general trends of deep-sea cused primarily on tropical species (Simpson 2009), coral reproduction, and these are fundamental to max- and there is currently an initiative towards reviewing imizing outcomes and economizing effort when plan- the literature on this subject (Kahng et al. 2008). How- ning new sampling initiatives. *Email: [email protected] © Inter-Research 2009 · www.int-res.com 104 Mar Ecol Prog Ser 397: 103–112, 2009 For general reproductive patterns in deep-sea corals, ing to 6 families, along the Brazilian coast. Seven of data exist primarily for groups such as scleractinians these recorded species came from depths below 200 m. (see review in Waller 2005), stylasterids (Brooke & The sea pen Anthoptilum murrayi Kölliker 1880 has Stone 2007) and octocorals (review in Simpson 2009). been reported from the shelf to the upper continental In terms of the sexual status and mode of development, slope of the North Atlantic, the northern Mid-Atlantic most shallow-water scleractinians are hermaphroditic Ridge, Faraday Seamount, the Indian Ocean and and spawn gametes for external fertilization (Harrison & waters around New Zealand and Australia (Jungersen Wallace 1990). In contrast, the limited available data on 1904, Thomson & Henderson 1906, Deichmann 1936, the deep-sea scleractinians to date shows that most are Cryer et al. 2002, McFadden et al. 2006, Molodtsova et gonochoric broadcast spawners. The exceptions are the al. 2008, Mortensen et al. 2008, Cairns et al. 2009). The species that have polyps adapted for brooding, such as first specimens from the South Atlantic were collected the Antarctic cup corals, Flabellum spp. (Waller et al. off Brazil, from 13° to 22° S (Pinto 2008). Most often, 2008) and 3 species of Caryophyllia which are herm- several specimens were sampled in a single dredge aphroditic (Waller 2005, Waller et al. 2005). (up to 52 colonies per dredge), which suggests high Twelve deep-sea stylasterids, belonging to the gen- local densities. era Stylaster, Errinopora, Distichopora, Cyclohelia and The present study describes the main characteristics Criptelia were studied by Brooke & Stone (2007). All on the reproductive biology of a member of the family were gonochoric brooders, in contrast to the shallow- Anthoptilidae, which has been considered one of the water Stylaster roseus, which may be hermaphroditic most primitive of the pennatulaceans (Doulan 2008). (Brooke & Stone 2007). The gametogenesis in male and female colonies of Despite the ecological importance of cold-water octo- Anthoptilum murrayi is described and estimates of corals, there are few published studies on their repro- their high fecundity are presented. Results of their ductive processes (Cordes et al. 2001, Orejas et al. 2002, reproductive characteristics are compared with data 2007), although some studies have included various as- available from other corals, particularly for sea pens. pects on the reproduction of pennatulaceans (Chia & As noted by Edwards & Moore (2009), A. murrayi con- Crawford 1973, Eckelbarger et al. 1998, Tremblay et al. firmed the pattern of both gonochorism and broadcast 2004, Soong 2005, Edwards & Moore 2008, 2009). How- spawning, which may be conserved at the order level ever, only 2 studies have focused on deep-water sea pens in Pennatulaceans. (Kophobelemnon stelliferum, Rice et al. 1992, and Um- bellula lindahli, Tyler et al. 1995). Gonochorism is the dominant pattern found for octo- MATERIALS AND METHODS corals, with only a few alcyonacean taxa being herm- aphroditic, e.g. Sinularia exilis (Benayahu 1997) and Colonies were collected off Bahia and Espírito Santo some species of Heteroxenia and Xenia (Benayahu States between 13° and 21° S in 2000 during the Living 1991, 1997). The frequency of brooding versus broad- Resources in the Exclusive Economic Zone (REVIZEE) cast spawning in octocorals varies with taxonomic Score Central Project (see Lavrado & Ignácio 2006), order (Simpson 2009). All pennatulaceans studied to and in 2003 off Rio de Janeiro State (Campos Basin, 21° date are broadcast spawners. to 22° S) during the Campos Basin Deep-Sea Environ- Anthozoans, especially scleractinians and octocorals, mental Project/PETROBRAS (Ocean Prof I and II cam- are the most dominant macrobenthic group in some paigns) (see Falcão et al. 2006). Specimens were up to deep-sea areas off Brazil (Castro et al. 2006). The pen- 75 cm in height (Fig. 1) and were collected at depths natulaceans are common octocorals, living in sediment between 1051 and 1799 m using otter trawls. A rela- areas surrounding deep-sea coral habitats. The order tively large number of specimens were collected dur- Pennatulacea occurs in all oceans, and species are gen- ing sampling, but only a few of these colonies (n = 24) erally adapted to living on soft sediments (Williams were undamaged and still bore intact polyps suitable 1995). Pennatulids are characterized by an oozooid (the for study. The 24 colonies were collected in February persistent and modified primary polyp), a proximal (4 specimens), June (9), July (4) and August (7). muscular peduncle and a distal polyp-bearing rachis Gametogenesis was examined using histological (polyparium) with autozooids (polyps with 8 well-de- methods. All colonies were fixed and preserved in veloped tentacles and mesenteries) and siphonozooids 70% alcohol, as they had been primarily collected for (polyps a with strongly developed siphonoglyph and taxonomic studies. The use of alcohol-preserved spec- reduced or absent tentacles) (Bayer et al. 1983). imens for histology was far from ideal and posed many The group has approximately 200 species (Williams, limitations during the various histological procedures. 1995). Castro & Medeiros (2001) and Castro et al. Tissues were fragile from alcohol preservation and the (2006) recorded 13 species of pennatulaceans, belong- process of extending the sections prior to application to Pires et al.: Reproduction of Anthoptilum murrayi 105
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